Evolution of the tumor suppressor BRCA1 locus in primates: Implications for cancer predisposition

Human Molecular Genetics

Volumn 13, Issue 22, 2004, Pages 2737-2751

  Pavlicek, Adam ^a   Noskov, Vladimir N ^b   Kouprina, Natalay ^b   Barrett, J Carl ^b   Jurka, Jerzy ^a   Larionov, Vladimir ^b  

^a Genetic Information Research Institute   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BREAST CANCER; CANCER SUSCEPTIBILITY; CHIMPANZEE; CONTROLLED STUDY; DNA TRANSPOSITION; EVOLUTIONARY HOMOLOGY; EXON; FRAMESHIFT MUTATION; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE LOCUS; GENE MUTATION; GENE REARRANGEMENT; GENETIC ANALYSIS; GENETIC CODE; GENETIC PREDISPOSITION; GENETIC SELECTION; GENETIC VARIABILITY; GERM LINE; GORILLA; MISSENSE MUTATION; MOLECULAR CLONING; NONHUMAN; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; ORANG UTAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SPECIES COMPARISON; TUMOR SUPPRESSOR GENE;

ALU ELEMENTS; AMINO ACID SEQUENCE; ANIMALS; BRCA1 PROTEIN; BREAST NEOPLASMS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; EXONS; FEMALE; GENE REARRANGEMENT; GENES, BRCA1; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; OVARIAN NEOPLASMS; PHOSPHORYLATION; PRIMATES; PROTEIN STRUCTURE, TERTIARY;

ANTHROPOIDEA; PAN TROGLODYTES; PRIMATES;

EID: 9544220659     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddh301     Document Type: Article

References (69)

1. Futreal, P.A., Liu, Q., Shattuck-Eidens, D., Cochran, C., Harshman, K., Tavtigian, S., Bennett, L.M., Haugen-Strano, A., Swensen, J., Miki, Y. et al. (1994) BRCA1 mutations in primary breast and ovarian carcinomas. Science, 266, 120-122.
2. Miki, Y., Swensen, J., Shattuck-Eidens, D., Futreal, P.A., Harshman, K., Tavtigian, S., Liu, Q., Cochran, C., Bennett, L.M., Ding, W. et al. (1994) A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science, 266, 66-71.
3. King, M.C., Marks, J.H. and Mandell, J.B. for The New York Breast Cancer Study Group. (2003) Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science, 302, 643-646.
4. Smith, T.M., Lee, M.K., Szabo, C.I., Jerome, N., McEuen, M., Taylor, M., Hood, L. and King, M.C. (1996) Complete genomic sequence and analysis of 117 kb of human DNA containing the gene BRCA1. Genome Res. 6, 1029-1049.
5. Rosen, E.M., Fan, S., Pestell, R.G. and Goldberg, I.D. (2003) BRCA1 gene in breast cancer. J. Cell Physiol., 196, 19-41.
6. Welcsh, P.L. and King, M.C. (2001) BRCA1 and BRCA2 and the genetics of breast and ovarian cancer. Hum. Mol. Genet., 10, 705-713.
7. Koonin, E.V., Altschul, S.F. and Bork, P. (1996) BRCA1 protein products... Functional motifs... Nat. Genet., 13, 266-268.
8. Cantor, S.B., Bell, D.W., Ganesan, S., Kass, E.M., Drapkin, R., Grossman, S., Wahrer, D.C., Sgroi, D.C., Lane, W.S., Haber, D.A. and Livingston, D.M. (2001) BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell, 105, 149-160.
9. Puget, N., Torchard, D., Serova-Sinilnikova, O.M., Lynch, H.T., Feunteun, J., Lenoir, G.M. and Mazoyer, S. (1997) A 1-kb Alu mediated germ-line deletion removing BRCA1 exon 17. Cancer Res., 57, 828-831.
10. Petrij-Bosch, A., Peelen, T., van Vliet, M., van Eijk, R., Olmer, R., Drusedau, M., Hogervorst, F.B., Hageman, S., Arts, P.J., Ligtenberg, M.J. et al. (1997) BRCA1 genomic deletions are major founder mutations in Dutch breast cancer patients. Nat. Genet. 17, 341-345.
11. Monteiro, A.N., August, A. and Hanafusa, H. (1996) Evidence for a transcriptional activation function of BRCA1 C-terminal region. Proc. Natl Acad. Sci. USA, 93, 13595-13599.
12. Brzovic, P.S., Rajagopal, P., Hoyt, D.W., King, M.C. and Klevit, R.E. (2001) Structure of a BRCA1-BARD1 heterodimeric RING-RING complex. Nat. Struct. Biol., 8, 833-837.
13. Vallon-Christersson, J., Cayanan, C., Haraldsson, K., Loman, N., Bergthorsson, J.T., Brondum-Nielsen, K., Gerdes, A.M., Moller, P., Kristoffersson, U. et al. (2001) Functional analysis of BRCA1 C-terminal missense mutations identified in breast and ovarian cancer families. Hum. Mol. Genet., 10, 353-360.
14. Fleming, M.A., Potter, J.D., Ramirez, C.J., Ostrander, G.K. and Ostrander, E.A. (2003) Understanding missense mutations in the BRCA1 gene: an evolutionary approach. Proc. Natl Acad. Sci. USA, 100, 1151-1156.
15. Ramirez, C.J., Fleming, M.A., Potter, J.D., Ostrander, G.K. and Ostrander, E.A. (2004) Marsupial BRCA1: conserved regions in mammals and the potential effect of missense changes. Oncogene, 23, 1780-1788.
16. Huttley, G.A., Easteal, S., Southey, M.C., Tesoriero, A., Giles, G.G., McCredie, M.R., Hopper, J.L. and Venter, D.J. (2000) Adaptive evolution of the tumour suppressor BRCA1 in humans and chimpanzees. Australian breast cancer family study. Nat. Genet., 25, 410-413.
17. Kouprina, N. and Larionov, V. (2003) Exploiting the yeast Saccharomyces cerevisiae for the study of the organization and evolution of complex genomes. FEMS Microbiol. Rev., 27, 629-649.
18. Brown, M.A., Lo, L.J., Catteau, A., Xu, C.F., Lindeman, G.J., Hodgson, S. and Solomon, E. (2002) Germline BRCA1 promoter deletions in UK and Australian familial breast cancer patients: Identification of a novel deletion consistent with BRCA1:psi BRCA1 recombination. Hum. Mutat., 19, 435-442.
19. Puget, N., Gad, S., Perrin-Vidoz, L., Sinilnikova, O.M., Stoppa-Lyonnet, D., Lenoir, G.M. and Mazoyer, S. (2002) Distinct BRCA1 rearrangements involving the BRCA1 pseudogene suggest the existence of a recombination hot spot. Am. J. Hum. Genet., 70 858-865.
20. Goodman M. (1999) The genomic record of Humankind's evolutionary roots. Am. J. Hum. Genet., 64, 31-39.
21. Montagna, M., Santacatterina, M., Torri, A., Menin, C., Zullato, D., Chieco-Bianchi, L. and D'Andrea, E. (1999) Identification of a 3 kb Alu-mediated BRCA1 gene rearrangement in two breast/ovarian cancer families. Oncogene, 18, 4160-4165.
22. Puget, N., Sinilnikova, O.M., Stoppa-Lyonnet, D., Audoynaud, C., Pages, S., Lynch, H.T., Goldgar, D., Lenoir, G.M. and Mazoyer, S. (1999) An Alu-mediated 6-kb duplication in the BRCA1 gene: a new founder mutation? Am. J. Hum. Genet., 64, 300-302.
23. Puget, N., Stoppa-Lyonnet, D., Sinilnikova, O.M., Page, S., Lynch, H.T., Lenoir, G.M. and Mazoyer, S. (1999) Screening for germ-line rearrangements and regulatory mutations in BRCA1 led to the identification of four new deletions. Cancer Res., 59, 455-461.
24. Rohlfs, E.M., Chung, C.H., Yang, Q., Skrzynia, C., Grody, W.W., Graham, M.L. and Silverman, L.M. (2000) In-frame deletions of BRCA1 may define critical functional domains. Hum. Genet., 107, 385-390.
25. Rohlfs, E.M., Puget, N., Graham, M.L., Weber, B.L., Garber, J.E., Skrzynia, C., Halperin, J.L., Lenoir, G.M., Silverman, L.M. and Mazoyer, S. (2000) An Alu-mediated 7.1 kb deletion of BRCA1 exons 8 and 9 in breast and ovarian cancer families that results in alternative splicing of exon 10. Genes Chromosomes Cancer, 28 300-307.
26. Montagna, M., Dalla Palma, M., Menin, C., Agata, S., De Nicolo, A., Chieco-Bianchi, L. and D'Andrea, E. (2003) Genomic rearrangements account for more than one-third of the BRCA1 mutations in northern Italian breast/ovarian cancer families. Hum. Mol. Genet., 12, 1055-1061.
27. Hogervorst, F.B., Nederlof, P.M., Gille, J.J., McElgunn, C.J., Grippeling, M., Pruntel, R., Regnerus, R., van Welsem, T., van Spaendonk, R., Menko, F.H. et al. (2003) Large genomic deletions and duplications in the BRCA1 gene identified by a novel quantitative method. Cancer Res., 63, 1449-1453.
28. Swensen, J., Hoffman, M., Skolnick, M.H. and Neuhausen, S.L. (1997) Identification of a 14 kb deletion involving the promoter region of BRCA1 in a breast cancer family. Hum. Mol. Genet., 6 1513-1517.
29. Abel, K.J., Xu, J., Yin, G.Y., Lyons, R.H., Meisler, M.H. and Weber, B.L. (1995) Mouse BRCA1: localization sequence analysis and identification of evolutionarily conserved domains. Hum. Mol. Genet. 4, 2265-2273.
30. Szabo, C.I., Wagner, L.A., Francisco, L.V., Roach, J.C., Argonza, R., King, M.C. and Ostrander, E.A. (1996) Human, canine and murine BRCA1 genes: sequence comparison among species. Hum. Mol. Genet., 5, 1289-1298.
31. Orelli, B.J., Logsdon, J.M., Jr and Bishop. D.K. (2001) Nine novel conserved motifs in BRCA1 identified by the chicken orthologue. Oncogene, 20, 4433-4438.
32. Yang, Z. and Nielsen, R. (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol., 19, 908-917.
33. Shen, D. and Vadgama, J.V. (1999) BRCA1 and BRCA2 gene mutation analysis: visit to the Breast Cancer Information Core (BIC). Oncol. Res. 11, 63-69.
34. Williams, R.S., Green, R. and Glover, J.N. (2001) Crystal structure of the BRCT repeat region from the breast cancer-associated protein BRCA1. Nat. Struct. Biol., 8, 838-842.
35. Brzovic, P.S., Meza, J.E., King, M.C. and Klevit, R.E. (2001) BRCA1 RING domain cancer-predisposing mutations. Structural consequences and effects on protein-protein interactions. J. Biol. Chem., 276 41399-41406.
36. Joo, W.S., Jeffrey, P.D., Cantor, S.B., Finnin, M.S., Livingston, D.M. and Pavletich, N.P. (2002) Structure of the 53BP1 BRCT region bound to p53 and its comparison to the BRCA1 BRCT structure. Genes Dev., 16, 583-593.
37. Okada, S. and Ouchi, T. (2003) Cell cycle differences in DNA damage-induced BRCA1 phosphorylation affect its subcellular localization. J. Biol. Chem., 278, 2015-2020.
38. Rodenhiser, D., Chakraborty, P., Andrews, J., Ainsworth, P., Mancini, D., Lopes, E. and Singh, S. (1996) Heterogenous point mutations in the BRCA1 breast cancer susceptibility gene occur in high frequency at the site of homonucleotide tracts, short repeats and methylatable CpG/CpNpG motifs. Oncogene, 12, 2623-2629.
39. Liu, H.X., Cartegni, L., Zhang, M.Q. and Krainer, A.R. (2001) A mechanism for exon skipping caused by nonsense or missense mutations in BRCA1 and other genes. Nat. Genet., 27, 55-58.
40. Perrin-Vidoz, L., Sinilnikova, O.M., Stoppa-Lyonnet, D., Lenoir, G.M. and Mazoyer, S. (2002) The nonsense-mediated mRNA decay pathway triggers degradation of most BRCA1 mRNAs bearing premature termination codons. Hum. Mol. Genet., 11, 2805-2814.
41. Ng, P.C. and Henikoff, S. (2003) SIFT: Predicting amino acid changes that affect protein function. Nucl. Acids Res., 31, 3812-3814.
42. Kouprina, N., Pavlicek, A., Mochida, G.H., Solomon, G., Gersch, W., Yoon, Y.H., Collura, R., Ruvolo, M., Barrett, J.C., Woods, C.G. et al. (2004) Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion. PLoS Biol., 5, 1-11.
43. Kapitonov, V.V., Pavlicek, A. and Jurka, J. (2004) Anthology of human repetitive DNA. In Meyers, R.A. (ed.) Encyclopedia of Molecular Cell Biology and Molecular Medicine. Wiley-VCH, Vol. 1, pp. 251-305.
44. Frolov, A., Prowse, A.H., Vanderveer, L., Bove, B., Wu, H. and Godwin, A.K. (2002) DNA array-based method for detection of large rearrangements in the BRCA1 gene. Genes Chromosomes Cancer, 35, 232-241.
45. Endo, T., Ikeo, K. and Gojobori T. (1996) Large-scale search for genes on which positive selection may operate. Mol. Biol. Evol. 13, 685-690.
46. Kreitman, M. and Comeron, J.M. (1999) Coding sequence evolution. Curr. Opin. Genet. Dev., 9, 637-641.
47. Cantor, S., Drapkin, R., Zhang, F., Lin, Y., Han, J., Pamidi, S. and Livingston, D.M. (2004) The BRCA1-associated protein BACH1 is a DNA helicase targeted by clinically relevant inactivating mutations. Proc. Natl Acad. Sci. USA, 101, 2357-2362.
48. Waterston, R.H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J.F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M., An, P. et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature, 420, 520-562.
49. Kondrashov, A.S., Sunyaev, S. and Kondrashov, F.A. (2002) Dobzhansky-Muller incompatibilities in protein evolution. Proc. Natl Acad. Sci. USA, 99, 14878-14883.
50. Gao, L. and Zhang, J. (2003) Why are some human disease-associated mutations fixed in mice? Trends. Genet., 19 678-681.
51. Annab, L.A., Kouprina, N., Solomon, G., Cable, P.L., Hill, D.E., Barrett, J.C., Larionov, V. and Afshari, C.A. (2000) Isolation of a functional copy of the human BRCA1 gene by transformation-associated recombination in yeast. Gene, 250, 201-208.
52. Kouprina, N. and Larionov, V. (1999) Selective isolation of mammalian genes by TAR cloning. In Dracopoli, N.C., Haines, J.L., Korf, B.R., Moir, D.T., Morton, C.C., Seidman, C.E., Seidman, J.G. and Smith, D.R. (eds) Current Protocols in Human Genetics. John Wiley & Sons, Vol. 1, pp. 5.17.1-5.17.21.
53. Polushin, N., Malykh, A., Malykh, O., Zenkova, M., Chumakova, N., Vlassov, V. and Kozyavkin, S. (2001) 2′-modified oligonucleotides from methoxyoxalamido and succinimido precursors: synthesis, properties, and applications. Nucleosides Nucleotides Nucl. Acids, 4-7, 507-511.
54. Bray, N. and Pachter, L. (2004) MAVID: Constrained Ancestral Alignment of Multiple Sequences. Genome Res., 14, 693-699.
55. Morgenstern, B. (1999) DIALIGN 2: improvement of the segment-to-segment approach to multiple sequence alignment. Bioinformatics, 15, 211-218.
56. Galtier, N., Gouy, M. and Gautier, C. (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci., 12, 543-548.
57. Rice, P., Longden, I. and Bleasby, A. (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends. Genet., 16, 276-277.
58. Jurka, J., Klonowski, P., Dagman, V. and Pelton, P. (1996) CENSOR-a program for identification and elimination of repetitive elements from DNA sequences. Comput. Chem., 20, 119-121.
59. Jurka, J. (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet., 16, 418-420.
60. Benson, G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucl. Acids Res., 27, 573-580.
61. Kent, W.J. (2002) BLAT - the BLAST-like alignment tool. Genome Res., 12, 656-664.
62. Korber, B. (2000) HIV signature and sequence variation analysis. In Rodrigo, A.G. and Learn, G.H. (eds) Computational Analysis of HIV Molecular Sequences. Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 55-72.
63. Gonnet, G.H., Cohen, M.A. and Benner, S.A. (1992) Exhaustive matching of the entire protein sequence database. Science, 256 1443-1145.
64. Szabo, C., Masiello, A., Ryan, J.F. and Brody, L.C. (2000) The breast cancer information core: database design, structure, and scope. Hum. Mutat., 16, 123-131.
65. Yang, Z. (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci., 13, 555-556.
66. Page, R.D.M. (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci., 12, 357-358.
67. Hohenstein, P. and Fodde, R. (2004) Of mice and (wo)men: genotype-phenotype correlations in BRCA1. Hum. Mol. Genet., 12 R271 -R277.
68. Hohenstein, P. (2004) Tumor Suppressor Genes in Tumorigenesis. PhD thesis, Leiden University, The Netherlands.
69. Yang, Z. (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol., 15, 568-573.